Toxoplasma gondii and Psychopathology: Latent Infection Is Associated with Interpersonal Sensitivity, Psychoticism, and Higher Testosterone Levels in Men, but Not in Women

Adaptive Human Behavior and Physiology - Tập 7 Số 1 - Trang 28-42 - 2021
Javier I. Borráz-León1, Markus J. Rantala1, Severi Luoto2, Indriķis Krams3, Jorge Contreras‐Garduño4, Ana Lilia Cerda-Molina5, Tatjana Krama6
1Department of Biology, University of Turku, Turku, Finland
2English, Drama and Writing Studies, University of Auckland, Auckland, New Zealand
3Institute of Systematic Biology, Daugavpils University, Daugavpils, Latvia
4Evolutionary Ecology Lab, ENES, National Autonomous University of Mexico, Morelia, Mexico
5Department of Ethology, National Institute of Psychiatry "Ramón de la Fuente Muñiz", Mexico City, Mexico
6Department of Biotechnology, Daugavpils University, Daugavpils, Latvia

Tóm tắt

Abstract Objective The ability of parasites to hijack the nervous system, manipulating the host’s physiology and behavior in ways that enhance the parasite’s fitness while damaging host fitness, is a topic of ongoing research interest in evolutionary biology, but is largely overlooked in mental health research. Nevertheless, recent evidence has shown that Toxoplasma gondii infection can change host testosterone levels and influence the development of some psychiatric disorders. Here, we tested this hypothesis in a mixed sample of 213 non-clinical subjects. Methods Participants (nmales = 108, nfemales = 105) provided 5 ml of blood to quantify testosterone levels and Toxoplasma gondii antibodies. The Symptom Checklist-90-Revised was used to assess psychopathological symptoms. Results The results showed that Toxoplasma-infected men had higher testosterone levels and scored higher in Interpersonal Sensitivity and Psychoticism symptoms than non-infected men. Toxoplasma-infected women did not differ from control women. Conclusions Framed in an evolutionary framework, the findings suggest that the elevated testosterone levels and the expression of psychopathological symptoms can be seen as the result of the manipulation exerted by Toxoplasma gondii either to reach its definitive host or to increase its spread. Future research can benefit from integrating insights from evolutionary biology and parasite-host interactions with physiology, immunology, and mental health to develop a better understanding of mental health etiology.

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Tài liệu tham khảo

Arantes, T. P., Lopes, W. D. Z., Ferreira, R. M., Pieroni, J. S. P., Pinto, V. M., Sakamoto, C. A., & da Costa, A. J. (2009). Toxoplasma gondii: Evidence for the transmission by semen in dogs. Experimental Parasitology, 123, 190–194. https://doi.org/10.1016/j.exppara.2009.07.003.

Barch, D. M., Shirtcliff, E. A., Elsayed, N. M., Whalen, D., Gilbert, K., Vogel, A. C., Tillman, R., & Luby, J. L. (2020). Testosterone and hippocampal trajectories mediate the relationship of poverty to emotion dysregulation and depression. Proceedings of the National Academy of Sciences, 117, 22015–22023. https://doi.org/10.1073/pnas.2004363117.

Berdoy, M., Webster, J. P., & Macdonald, D. W. (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society B: Biological Sciences, 267, 1591–1594. https://doi.org/10.1098/rspb.2000.1182.

Booth, A., Johnson, D. R., & Granger, D. A. (1999). Testosterone and men’s depression: the role of social behavior. Journal of Health and Social Behavior, 40, 130–140.

Borráz-León, J. I., & Rantala, M. J. (2021). Does the Dark Triad predict self-perceived attractiveness, mate value, and number of sexual partners both in men and women? Personality and Individual Differences, 168, 110341. https://doi.org/10.1016/j.paid.2020.110341.

Borráz-León, J. I., Cerda-Molina, A. L., Choi, D., & Mayagoitia-Novales, L. (2018). Testosterone and intrasexual competition in men: Is there any relationship with digit ratio (2D:4D)? Acta Ethologica, 21, 137–140. https://doi.org/10.1007/s10211-018-0284-9.

Boyce, P., & Parker, G. (1989). Development of a scale to measure interpersonal sensitivity. Australian & New Zealand Journal of Psychiatry, 23, 341–351. https://doi.org/10.3109/00048678909068294.

Brüne, M. (2019). Latent toxoplasmosis: host-parasite interaction and psychopathology. Evolution, Medicine, and Public Health, 2019, 212–213. https://doi.org/10.1093/emph/eoz032.

Cicchetti, D. (2016). Socioemotional, personality, and biological development: Illustrations from a multilevel developmental psychopathology perspective on child maltreatment. Annual Review of Psychology, 67, 187–211. https://doi.org/10.1146/annurev-psych-122414-033259.

Cobey, K. D., Nicholls, M., Leongómez, J. D., & Roberts, S. C. (2015). Self-reported dominance in women: Associations with hormonal contraceptive use, relationship status, and testosterone. Adaptive Human Behavior and Physiology, 1, 449–459. https://doi.org/10.1007/s40750-015-0022-8.

Cook, T. B., Brenner, L. A., Cloninger, C. R., Langenberg, P., Igbide, A., Giegling, I., Hartmann, A. M., Konte, B., Friedl, M., Brundin, L., Groer, M. W., Can, A., Rujescu, D., & Postolache, T. T. (2015). “Latent” infection with Toxoplasma gondii: association with trait aggression and impulsivity in healthy adults. Journal of Psychiatric Research, 60, 87–94. https://doi.org/10.1016/j.jpsychires.2014.09.019.

Costa, R. M., Correia, M., & Oliveira, R. F. (2015). Does personality moderate the link between women’s testosterone and relationship status? The role of extraversion and sensation seeking. Personality and Individual Differences, 76, 141–146. https://doi.org/10.1016/j.paid.2014.12.003.

Cruz Fuentes, C. S., López Bello, L., Blas García, C., González Macías, L., & Chávez, Balderas, R. A. (2005). Datos sobre la validez y confiabilidad de la Symptom Check List 90 (SCL-90) en una muestra de sujetos mexicanos. Salud Mental, 28, 72–81.

Dass, S. A. H., Vasudevan, A., Dutta, D., Soh, L. J. T., Sapolsky, R. M., & Vyas, A. (2011). Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness on males. PLoS ONE, 6, e27229. https://doi.org/10.1371/journal.pone.0027229.

Dawkins, R. (1982). The extended phenotype: The long reach of the gene. Oxford: Oxford University Press.

Del Giudice, M. (2014). An evolutionary life history framework for psychopathology. Psychological Inquiry, 25, 261–300. https://doi.org/10.1080/1047840X.2014.884918.

Del Giudice, M. (2017). Mating, sexual selection, and the evolution of schizophrenia. World Psychiatry, 16, 141. https://doi.org/10.1002/wps.20409.

Del Giudice, M. (2019). Invisible designers: Brain evolution through the lens of parasite manipulation. The Quarterly Review of Biology, 94, 249–282. https://doi.org/10.1086/705038.

Del Giudice, M. D., & Ellis, B. J. (2016). Evolutionary foundations of developmental psychopathology. Developmental Psychopathology, 1–58. https://doi.org/10.1002/9781119125556.devpsy201

Derogatis, L. R., & Unger, R. (2010). Symptom checklist-90-revised. The Corsini encyclopedia of psychology, 1–2. https://doi.org/10.1002/9780470479216.corpsy0970

Eisenegger, C., Haushofer, J., & Fehr, E. (2011). The role of testosterone in social interaction. Trends in Cognitive Sciences, 15, 263–271. https://doi.org/10.1016/j.tics.2011.04.008.

Figueira, M. L., & Ouakinin, S. (2010). Gender-related endocrinological dysfunction and mental disorders. Current Opinion in Psychiatry, 23, 369–372. https://doi.org/10.1097/YCO.0b013e3283399b86.

Flegr, J. (2007). Effects of Toxoplasma on human behavior. Schizophrenia Bulletin, 33, 757–760. https://doi.org/10.1093/schbul/sbl074.

Flegr, J. (2013). How and why Toxoplasma makes us crazy. Trends in Parasitology, 29, 156–163. https://doi.org/10.1016/j.pt.2013.01.007.

Flegr, J., & Horáček, J. (2019). Negative effects of latent toxoplasmosis on mental health. Frontiers in Psychiatry, 10, 1012. https://doi.org/10.3389/fpsyt.2019.01012.

Flegr, J., Preiss, M., Klose, J., Havlíček, J., Vitáková, M., & Kodym, P. (2003). Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii Dopamine, a missing link between schizophrenia and toxoplasmosis? Biological Psychology, 63, 253–268. https://doi.org/10.1016/S0301-0511(03)00075-9.

Flegr, J., Lindová, J., & Kodym, P. (2008). Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology, 135, 427–431. https://doi.org/10.1017/S0031182007004064.

Flegr, J., Lenochová, P., Hodný, Z., & Vondrová, M. (2011). Fatal attraction phenomenon in humans-cat odour attractiveness increased for Toxoplasma-infected men while decreased for infected women. PLOS Neglected Tropical Diseases, 5, e1389. https://doi.org/10.1371/journal.pntd.0001389.

Frayer, D. W. (1980). Sexual dimorphism and cultural evolution in the late Pleistocene and Holocene of Europe. Journal of Human Evolution, 95, 399–415. https://doi.org/10.1016/0047-2484(80)90050-0.

Geffre, A. C., Liu, R., Manfredini, F., Beani, L., Kathirithamby, J., Grozinger, C. M., & Toth, A. L. (2017). Transcriptomics of an extended phenotype: Parasite manipulation of wasp social behaviour shifts expression of caste-related genes. Proceedings of the Royal Society B: Biological Sciences, 284, 20170029. https://doi.org/10.1098/rspb.2017.0029.

Giammanco, M., Tabacchi, G., Giammanco, S., Di Majo, D., & La Guardia, M. (2005). Testosterone and aggressiveness. Medical Science Monitor, 11. In RA136–RA145.

Hlaváčová, J., Flegr, J., Řežábek, K., Calda, P., & Kaňková, Š. (2020). Male-to-Female presumed transmission of Toxoplasmosis between sexual partners. American Journal of Epidemiology, Kwaa 198. https://doi.org/10.1093/aje/kwaa198

Hsu, P. C., Groer, M., & Beckie, T. (2014). New findings: depression, suicide, and Toxoplasma gondii infection. Journal of the American Association of Nurse Practitioners, 26, 629–637. https://doi.org/10.1002/2327-6924.12129.

Hull, E. M., Muschamp, J. W., & Sato, S. (2004). Dopamine and serotonin: influences on male sexual behavior. Physiology and Behavior, 83, 291–307. https://doi.org/10.1016/j.physbeh.2004.08.018.

Kaňková, Š., Šulc, J., Nouzová, K., Fajfrlík, K., Frynta, D., & Flegr, J. (2007). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften, 94, 122–127. https://doi.org/10.1007/s00114-006-0166-2.

Kaňková, Š., Kodym, P., & Flegr, J. (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Experimental Parasitology, 128, 181–183. https://doi.org/10.1016/j.exppara.2011.03.014.

Khera, M. (2013). Patients with testosterone deficiency syndrome and depression. Archivos Españoles de Urologia, 66, 729–736.

Lara, M. A., Navarrete, L., Nieto, L., & Le, H. N. (2015). Childhood abuse increases the risk of depressive and anxiety symptoms and history of suicidal behavior in Mexican pregnant women. Brazilian Journal of Psychiatry, 37, 203–210. https://doi.org/10.1590/1516-4446-2014-1479.

LeBoutillier, N., Barry, R., & Westley, D. (2016). Creativity and the measurement of subclinical psychopathology in the general population: Schizotypy, psychoticism, and hypomania. Psychology of Aesthetics, Creativity, and the Arts, 10, 240–247. https://doi.org/10.1037/aca0000047.

Lim, A., Kumar, V., Dass, S. A. H., & Vyas, A. (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Molecular Ecology, 22, 102–110. https://doi.org/10.1111/mec.12042.

Liu, R. T., Kraines, M. A., Massing-Schaffer, M., & Alloy, L. B. (2014). Rejection sensitivity and depression mediation by stress generation. Psychiatry: Interpersonal and Biological Processes, 77, 86–97. https://doi.org/10.1521/psyc.2014.77.1.86.

Lodha, P., & Karia, S. (2019). Testosterone and schizophrenia: A clinical review. Annals of Indian Psychiatry, 3, 92–96. https://doi.org/10.4103/aip.aip_54_19.

Luoto, S. (2020). Sex differences in people and things orientation are reflected in sex differences in academic publishing. Journal of Informetrics, 14, 101021. https://doi.org/10.1016/j.joi.2020.101021.

Luoto, S., Krams, I., & Rantala, M. J. (2019). A life history approach to the female sexual orientation spectrum: Evolution, development, causal mechanisms, and health. Archives of Sexual Behavior, 48, 1273–1308. https://doi.org/10.1007/s10508-018-1261-0.

Maddux, J. E., & Winstead, B. A. (2015). Psychopathology: Foundations for a contemporary understanding. Routledge. https://doi.org/10.4324/9781315778945

Manning, N. (2019). Sociology, biology and mechanisms in urban mental health. Social Theory & Health, 17, 1–22. https://doi.org/10.1057/s41285-018-00085-7.

Marcinkowska, U. M., Helle, S., Jones, B. C., & Jasienska, G. (2019). Does testosterone predict women’s preference for facial masculinity? PloS ONE, 14, e0210636. https://doi.org/10.1371/journal.pone.0210636.

McCabe, R. E., Blankstein, K. R., & Mills, J. S. (1999). Interpersonal sensitivity and social problem-solving: Relations with academic and social self-esteem, depressive symptoms, and academic performance. Cognitive Therapy and Research, 23, 587–604. https://doi.org/10.1023/A:1018732707476.

Melcangi, R. C., Panzica, G., & Garcia-Segura, L. M. (2011). Neuroactive steroids: focus on human brain. Neuroscience, 191(1–5). https://doi.org/10.1016/j.neuroscience.2011.06.024.

Mitchell, K. R., Mercer, C. H., Prah, P., Clifton, S., Tanton, C., Wellings, K., & Copas, A. (2019). Why do men report more opposite-sex sexual partners than women? Analysis of the gender discrepancy in a British national probability survey. The Journal of Sex Research, 56, 1–8. https://doi.org/10.1080/00224499.2018.1481193.

Montoya, J., & Liesenfeld, O. (2004). Toxoplasmosis. Lancet, 363, 1965–1976. https://doi.org/10.1016/S0140-6736(04)16412-X.

Peters, M., Simmons, L. W., & Rhodes, G. (2008). Testosterone is associated with mating success but not attractiveness or masculinity in human males. Animal Behaviour, 76, 297–303. https://doi.org/10.1016/j.anbehav.2008.02.008.

Poirotte, C., Kappeler, P. M., Ngoubangoye, B., Bourgeois, S., Moussodji, M., & Charpentier, M. J. (2016). Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Current Biology, 26, R98–R99. https://doi.org/10.1016/j.cub.2015.12.020.

Rantala, M. J., Moore, F. R., Skrinda, I., Krama, T., Kivleniece, I., Kecko, S., & Krams, I. (2012). Evidence for the stress-linked immunocompetence handicap hypothesis in humans. Nature Communications, 3, 1–5. https://doi.org/10.1038/ncomms1696.

Rantala, M. J., Luoto, S., Krams, I., & Karlsson, H. (2018). Depression subtyping base on evolutionary psychiatry: Proximate mechanisms and ultimate functions. Brain, Behavior, and Immunity, 69, 603–617. https://doi.org/10.1016/j.bbi.2017.10.012.

Rantala, M. J., Luoto, S., Krama, T., & Krams, I. (2019). Eating disorders: An evolutionary psychoneuroimmunological approach. Frontiers in Psychology, 10, 2200. https://doi.org/10.3389/fpsyg.2019.02200.

Richards, G., Klimek, M., Jasienska, G., & Marcinkowska, U. M. (2018). Digit ratio (2D:4D) and circulating testosterone, oestradiol, progesterone levels across the menstrual cycle. Early Human Development, 117, 68–73. https://doi.org/10.1016/j.earlhumdev.2017.12.006.

Roberts, A., Hedman, K., Luyasu, V., Zufferey, J., Bessières, M. H., Blatz, R. M., Candolfi, E., Decoster, A., Enders, G., Gross, U., Guy, E., Hayde, M., Ho-Yen, D., Johnson, J., Lécolier, B., Naessens, A., Pelloux, H., Thulliez, P., & Petersen, E. (2001). Multicenter evaluation of strategies for serodiagnosis of primary infection with Toxoplasma gondii. European Journal of Clinical Microbiology and Infectious Diseases, 20, 467–474. https://doi.org/10.1007/PL00011289.

Roney, J. R., Simmons, Z. L., & Gray, P. B. (2011). Changes in estradiol predict within-women shifts in attraction to facial cues of men’s testosterone. Psychoneuroendocrinology, 36, 742–749. https://doi.org/10.1016/j.psyneuen.2010.10.010.

Silverman, I., Choi, J., & Peters, M. (2007). The hunter-gatherer theory of sex differences in spatial abilities: Data from 40 countries. Archives of Sexual Behavior, 36, 261–268. https://doi.org/10.1007/s10508-006-9168-6.

Skallová, A., Kodym, P., Frynta, D., & Flegr, J. (2006). The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethnopharmacological study. Parasitology, 133, 525–535. https://doi.org/10.1017/S0031182006000886.

Spauwen, J., Krabbendam, L., Lieb, R., Wittchen, H. U., & Van Os, J. (2006). Impact of psychological trauma on the development of psychotic symptoms: relationship with psychosis proneness. The British Journal of Psychiatry, 188, 527–533. https://doi.org/10.1192/bjp.bp.105.011346.

Szczypka, M. S., Zhou, Q. Y., & Palmiter, R. D. (1998). Dopamine-stimulated sexual behavior is testosterone dependent mice. Behavioral Neuroscience, 112, 1229–1235. https://doi.org/10.1037/0735-7044.112.5.1229.

Torrey, E. F., & Yolken, R. H. (2019). Schizophrenia as a pseudogenetic disease: A call for more gene-environmental studies. Psychiatry Research, 278, 146–150. https://doi.org/10.1016/j.psychres.2019.06.006.

Torrey, E. F., Bartko, J. J., Lun, Z. R., & Yolken, R. H. (2006). Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophrenia Bulletin, 33, 729–736. https://doi.org/10.1093/schbul/sbl050.

Urbán, R., Kun, B., Farkas, J., Paksi, B., Kökönyei, G., Unoka, Z., Felvinczi, K., Oláh, A., & Demetrovics, Z. (2014). Bifactor structural model of symptom checklists: SCL-90-R and Brief Symptom Inventory (BSI) in a non-clinical community simple. Psychiatry Research, 216, 146–154. https://doi.org/10.1016/j.psychres.2014.01.027.

van Anders, S. M., Hamilton, L. D., & Watson, N. V. (2007). Multiple partners are associated with higher testosterone in North American men and women. Hormones and Behavior, 51, 454–459. https://doi.org/10.1016/j.yhbeh.2007.01.002.

Webster, J. P. (2001). Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes and Infection, 3, 1037–1045. https://doi.org/10.1016/S1286-4579(01)01459-9.

Wedgeworth, M., LaRocca, M. A., Chaplin, W. F., & Scogin, F. (2017). The role of interpersonal sensitivity, social support, and quality of life in rural older adults. Geriatric Nursing, 38, 22–26. https://doi.org/10.1016/j.gerinurse.2016.07.001.

Welling, L. L., Jones, B. C., DeBruine, L. M., Conway, C. A., Smith, M. L., Little, A. C., & Al-Dujaili, E. A. (2007). Raised salivary testosterone in women is associated with increased attraction to masculine faces. Hormones and Behavior, 52, 156–161. https://doi.org/10.1016/j.yhbeh.2007.01.010.

Zouei, N., Shojaee, S., Mohebali, M., & Keshavarz, H. (2018). The association of latent toxoplasmosis and level of serum testosterone in humans. BMC Research Notes, 11, 365. https://doi.org/10.1186/s13104-018-3468-5.